Crying babies

‘My baby won’t stop crying doctor!’ - This presentation to a GP surgery can make even the more experienced practitioner feel uneasy. The complaint is non-specific with a broad range of differential diagnoses including severe or potentially life-threatening pathologies. Despite this, it is reassuring to know that in most cases, infant crying is not only a benign but also a normal behaviour. This article will discuss how to distinguish normal infant crying from a pathological cause and subsequent management approaches.


Why do babies cry?
Babies in early infancy will cry for a multitude of reasons. It can occur as an innate physiological response to either physical or environmental stimuli such as a wet nappy or hunger, or being too hot or too cold. However, often parents will have checked for any possible resolvable cause of crying and still find the baby continues to be inconsolable.
It has been hypothesised that in early infancy, crying with no apparent cause can be part of normal behavioural development. Only after this point does it becomes more purposeful and one of several developing methods of communication (Barr, 2004).
An increase in the length of time a well-baby spends crying each day is often seen from around 2 weeks of age. The peak of infant crying usually occurs at about 6-8 weeks of age, with subsequent improvement by about 4 months. Within this distribution over time, some babies will be particularly 'high criers' -crying for 5-6 hours per day at 6-8 weeks. Other babies' peak will be much less (20-30 minutes per day). This has been previously described as 'The curves of early infant crying' as seen in Fig. 1 (Barr et al., 2000).

When does crying become 'colic'?
Infantile colic is defined as a 'self-limiting condition' characterised by 'repeated episodes of excessive and inconsolable crying in an infant that otherwise appears to be healthy and thriving' (National Institute for Health and Care Excellence (NICE), 2017). The key part of this definition that distinguishes colic from normal infant crying is that colic is 'excessive' crying. For research purposes 'excessive crying' is said to be more than 3 hours a day, three times per week for more than 1 week (Benninga et al., 2016). In practice, the parents' or carers' perception that the crying is excessive is more relevant than the specific time duration each day.
The worldwide prevalence of colic has been estimated to be approximately 20%. However, there is a lack of good quality data (Vandenplas et al., 2015). The pathophysiology of colic also remains somewhat of a mystery. There are several suggested aetiologies, to name a few: feeding technique, poor gastrointestinal absorption, abnormalities in gut motility, differences in gut microbiome and an imbalance of the central nervous system (Akhnikh et al., 2014). It is important to recognise that psychosocial factors may play a part. These may include parental anxiety and perception of crying. This will be discussed in more detail. Evidence remains inconclusive on one particular cause, and it is generally accepted that it is probably multifactorial.
Arguably it could be said that colic as a term is unhelpful and 'colicky babies' should instead be more simply regarded as being on the higher end of the spectrum of normal infant crying. Regardless of the terminology, we do know that 'colic' is self-limiting, and as with the curves of normal crying, an improvement is seen by 4-5 months. It is generally regarded as benign, with no proven long-term repercussions. Several small studies on whether there are medical, psychological or behavioural consequences of infant colic have had inconclusive or contradictory results (Vandenplas et al., 2015).
Although this is reassuring for doctors and parents alike, it is important to remember that there are multiple other causes for a crying baby including potentially pathological causes. These should be excluded through a full history and examination.

History and examination
The first consideration when reviewing a crying baby is -is this child acutely unwell? There are several red flag symptoms that warrant an immediate referral to the children's emergency department for review (Box 1).
Once it has been established that the child is not acutely unwell, the second consideration is whether a medical cause can be found for crying or whether this is part of a normal behavioural pattern. When taking a history from the parent or carer it is often helpful to structure the history around the possible causes.

Hunger
The aim of this part of the history is to get an idea of whether or not the baby could be hungry: . Is the baby bottle or breast-fed?
. How often is the baby feeding? Is the baby waking for feeds? If the child is breast-fed -how long are they spending on each breast? -Milk produced during a breastfeed changes consistency during the feed. The milk thickens as the feed continues, with a higher proportion of calorific fats towards the end. Mothers therefore should be encouraged to fully feed from one breast at a time to ensure the baby is getting this higher calorie milk . Breast-fed babies are often fed responsively, for example when the baby shows signs of hunger. Bottle-fed babies tend to be fed on a pre-scheduled regimen. Regardless of the route they are fed, very young babies should be fed around every 3 hours, including overnight . If the child is bottle-fed, it is important to calculate how much the baby is being given -it should be 150-200 ml/ kg/day Midwives and health visitors can assist with feeding assessments and support parents. Unicef's baby friendly initiative also has helpful information for professionals and parents on breast and bottle feeding (Unicef, 2019).

Overstimulation/tiredness
Is the baby showing signs of tiredness? Signs may include frowning, clenched hands or crying. It is useful to consider how much the infant is sleeping in a 24-hour period. Studies have produced no clear consensus on how much sleep a baby Sudden onset of crying and irritability or a high-pitched or altered cry Fever or other concerns of sepsis or meningitis -for example, a non-blanching rash Increasing head size, hypertension or a bulging fontanelle Concern about dehydration Apnoeic episodes or evidence of respiratory distress Change in behaviour -for example, lethargy, not waking for feeds and reduced responsiveness Bilious, projectile or excessive vomiting; blood in the stool or vomit Concerns over the mental state of a parent or carer, or concern about a non-accidental injury of less than 4 months requires (Watson et al., 2015). As a guide, NHS Choices report a 4-week-old baby will require approximately 6-7 hours during the day and 8-9 hours at night. At 12-weeks, an infant will require 4-5 hours and 10-11 hours respectively (NHS Choices, 2017).

Colic
Despite cynicism around the validity of colic as a distinct diagnosis (rather than it being simply the higher end of the spectrum of normal crying), there are certain features that have been attributed to it. These include babies that are more unsettled in the afternoon and evening, and babies that draw their legs up to their chest while crying, clench their fists or go red in the face (NHS, 2018).

Parental and carer health
Assessing parents of crying babies for psychosocial risk factors and perinatal anxiety and depression is essential. Both parents should be asked about their current mental state, whether there is any past history of mental health problems and what social supports they have in place.
Depression and psychosocial stressors can impair the parent or carer's ability to sooth the child resulting in a cycle of worsening crying and parental stress. It is widely known there are higher maternal depression rates in mothers of crying babies. Sadly, high levels of infant crying are a recognised risk factor for abusive head trauma (shaken baby syndrome). Assessing parents' or carers' mental health and offering support is of vital importance. This will be discussed later in this article.

Pathological cause
As seen in Table 1 the differentials for pathological causes of crying in babies are broad and a full systems review is required: . Clarify when the parents first noted the crying to increase and whether there is any clear precipitant or pattern . Check whether the nature of the cry has changed, for example in a baby with meningitis the parents will often describe a high-pitched cry . Ask about signs of infection, for example a fever . Ask about stool pattern and bilious vomiting . Discuss feeding history as described above including if the baby is waking for feeds and clarifying that the baby is having regular wet nappies . It is important to directly ask parents or carers if the baby has sustained any injuries as they may not spontaneously disclose this fact Complete the history by discussing the antenatal and perinatal period, medications, immunisation status and social history.

Examination
It is important for a full examination to be performed, even if the baby is asleep and settled. This should involve fully exposing the baby and checking under the nappy. It is important to note their overall appearance and the interaction between the parents and the infant. The infant needs a full set of observations including a temperature and a blood pressure if an appropriately sized cuff is available. An up-to-date weight and head circumference should also be plotted on a growth chart. It is helpful if the parents have their 'red book' so the trend in growth can be seen.
Specifics for examination of the crying baby are detailed in Box 2. In infants presenting routinely for the postnatal check the examination might be combined. However, a full description of the 6-week check examination is beyond the scope of this article.

Gastro-oesophageal reflux
Uncomplicated gastro-oesophageal reflux is very common in infants for several reasons, including an anatomical predisposition and a purely liquid diet. Most do not require any treatment (Lightdale and Gremse, 2013) and full resolution occurs by 12-18 months (Russell, 2015). Gastro-oesophageal reflux disease (GORD) occurs when troublesome symptoms or complications occur due to reflux (Rosen et al., 2018 The diagnosis of GORD in infants almost always relies on the clinical history and examination findings. A challenge is that many of the recognised symptoms of GORD can also be attributed to normal infant behaviour -for example, excessive crying, back-arching and regurgitation. Importantly, in the absence of other symptoms of reflux, excessive crying alone is unlikely to be due to GORD (Heine et al., 2006). It would, therefore, be prudent to avoid starting unnecessary anti-reflux medications. Indeed, NICE recommend a diagnosis of GORD should only be considered if regurgitation is a feature unless there are multiple other symptoms of GORD as described above (NICE, 2016).
Most cases of GORD can be managed in primary care and a stepwise approach should be followed. In an otherwise healthy and thriving infant, parents can be reassured, and the initial management can be through conservative measures. This would include ensuring the baby is positioned correctly before and after feeds. In bottle-fed babies, appropriate feed volumes and frequency should be considered. As previously discussed, the health visitor and midwifery teams are a great resource and experienced both in feeding assessments and supporting parents.
If there is no improvement with conservative measures in a formula-fed infant, the next step would be giving thickened feeds. Pre-thickened formulas or thickeners are available. If this is not effective, they should be stopped and a 2-week Box 2. Examination.

General condition
Is the baby alert, warm and well-perfused? Check the skin turgor, the mucous membranes and the central capillary refill time. Does the baby handle well or are they irritable when touched?

Developmental and neurological
Check to see if the infant is smiling responsively and fixing to and following moving objects or faces. In a term babythe limit ages for these developmental milestones are 8 weeks and 3-months respectively. Around 6-8 weeks is the median age for which a term baby will be able to raise their heads to 45 when laid prone

Eyes
Consider corneal abrasion or a foreign body. Check the red reflex is present

Ears
Look for a retained foreign body -rare in this age group Mouth Look for oral thrush, burns from a hot bottle, or a torn frenulum. The latter is a red flag for a non-accidental injury. If there are concerns around feeding, check the suckling reflex and palpate the palate for any deformity

Chest
Listen for signs of pneumonia and pneumothorax. Check for normal heart sounds Abdomen Check the abdomen is soft and non-tender with no distension Nappy area Look for rashes, sores, anal fissures and a tight phimosis. It is also a good time to look for an incarcerated hernia or testicular torsion. The latter is rare, but can occasionally occur in infants.

Orthopaedic
All long bones should be examined. Bruising in nonmobile infants is always a red flag for non-accidental injury. An asymmetrical moro reflex is suggestive of a clavicle injury. All digits should be checked. Infants have small fingers and toes meaning there is a risk of developing a hair tourniquet. It is difficult to trim their nails, which may result in a paronychia

Skin
Careful examination of the skin may reveal areas of eczema. In an atopic child, this could indicate a non-IgEmediated cow's milk protein intolerance. Again, ensure there is no evidence of trauma trial of Gaviscon Infant commenced. In a breast-fed baby with no improvement following conservative measures a trial of Gaviscon Infant should be given. This should be continued if effective, but parents should be advised to stop treatment regularly to see if symptoms have improved and treatment may therefore be stopped (NICE, 2016).
If troublesome symptoms of GORD continue despite the above measures, a trial of a proton-pump inhibitor or a histamine-2 receptor antagonist may be appropriate. There is little evidence to suggest one class of drug is better in the management of GORD than the other (Lopez and Lemberg, 2019). The infant should be followed up after 4 weeks to assess the response. If symptoms still persist despite the above measures, then it would be reasonable to make a paediatric referral.
GORD symptoms may also be indistinguishable from those of cow's milk protein allergy (CMPA) (Ludman et al., 2013). CMPA should be considered in cases of severe or resistant GORD, particularly if co-existing allergic features are observed.

Cow's milk protein allergy
Although CMPA is more common in bottle-fed infants, it can also affect breast-fed babies. Features suggestive of CMPA include persistent crying, vomiting, diarrhoea or constipation (less common), blood in the stool, signs of atopy (eczema, wheeze), poor weight gain and feeding problems. CMPA can be either an immediate reaction (immunoglobulin E (IgE)-mediated), or a delayed reaction (non-IgE-mediated). Sometimes a mixed picture exists. An IgE-mediated reaction can be much easier to diagnose, as the infant will have symptoms usually within minutes to hours after exposure to cow's milk protein (Flom and Sicherer, 2019). Symptoms can include wheeze, urticarial rash and angio-oedema. The diagnosis of non-IgE-mediated CMPA can be more challenging, due to the variability in symptoms and the time they manifest after exposure. Excessive crying is a common feature in both non-IgE-mediated CMPA and infantile colic. CMPA should be considered in patients with persistent excessive crying in the setting of clinical features of CMPA. CMPA should also be considered in patients with eczema, GORD, and chronic gastrointestinal symptoms that are not responding to treatment (NICE, 2019).
Infants presenting with an IgE-mediated reaction should be referred to secondary care where allergy testing may take place. If the patient has not required immediate transfer to hospital, the urgency of referral will depend on clinical judgement. Management in the time between referral and review in secondary care depends on the method in which the infant is fed. If the infant is formula-fed, they should be trialled on an extensively-hydrolysed formula. If they are breast-fed, advice should be given on exclusion of dairy from the mother's diet (NICE, 2018).
The diagnosis of non-IgE CMPA is made through a 2-4week trial of eliminating cow's milk from an infant's diet. Breast-feeding mothers should be advised to go on a dairyfree exclusion diet and encouraged to continue breast-feeding. It is important to advise them to take supplementary vitamin D and calcium. Formula-fed infants should be trialled on extensively-hydrolysed cow's milk formula. If there is an improvement in symptoms following the exclusion trial period, reintroduction of cow's milk in the infant's diet can occur. If symptoms reoccur, the extensively-hydrolysed cow's milk formula or maternal exclusion diet should be restarted. If symptoms do not reoccur, the diagnosis is less likely to be CMPA. If there is no improvement of symptoms with the exclusion diet, trial with an amino acid formula could be considered. It is likely that specialist advice is needed at this point.
In the management of both IgE and non-IgE CMPA, a paediatric dietician referral is beneficial. In addition, a helpful resource for parents and professionals is the GP Infant Feeding Network (UK) (GP Infant Feeding Network, 2017). It is important to explain to parents that CMPA is usually transient, and most children develop tolerance to cow's milk protein by the time they are 3-years-old (Fiocchi et al., 2010).

Lactose intolerance
Lactose intolerance is a non-immune-mediated reaction to lactose in food due to the lack of the enzyme lactase. Primary lactose intolerance is extremely rare in infants. The most common cause of lactose intolerance is following a gastroenteritis infection that causes damage to the intestinal brush border where lactase enzymes are located (Brough and Nataraja, 2018). The symptoms of secondary lactose intolerance only usually last for between 4 and 6 weeks. Secondary lactose intolerance should be suspected in a crying baby with frothy and explosive loose stools and abdominal bloating following a gastroenteritis illness (Brough and Nataraja, 2018).
Where lactose intolerance is suspected; bottle-fed infants should be trialled on a lactose-free formula. Breast-fed babies should have lactase drops prescribed. Symptoms usually resolve within a few days following removal of lactose from the diet. As it is generally a transient condition, it is usually safe to re-introduce lactose into the infant's diet after 4-6 weeks.

Management of colic or normal infant crying
In most cases, no pathological cause will be found, and both parents and doctor can feel reassured that this is normal infant crying and will resolve with time. 'Job done. Next patient please . . ..' Not quite. It should not be considered so straight-forward. Despite the seemingly benign nature, infant colic can be extremely distressing for caregivers. Parents or caregivers may have ongoing anxiety that the baby is unwell or may feel the crying is a reflection of their parenting ability. This can be especially unsettling for new parents. Their distress is likely only exacerbated by the inevitable sleep deprivation that comes with looking after a new baby. As previously stated, infantile colic is a recognised risk factor for 'abusive head trauma' (shaken baby syndrome). Understandably, it is vitally important that parents or carers are not dismissed and supported appropriately to manage their infant's crying.
Suggested interventions include: . Acknowledging parental distress alongside reassurance that colic is benign and will resolve . Some comforting measures that could be tried: A warm bath Skin-to-skin contact Hum, sing or talk to your baby White noise Gentle rocking Take your baby out for a walk . Remind the parents that as long as the baby is in a safe place, it's fine to walk away and leave the room for a few minutes . If not already involved, refer the parents or carers to the health visitor team NICE clinical knowledge summary guidance recommends the following should not be recommended as there is 'insufficient good-quality evidence for their use' -simethicone or lactase drops, changing infant formula or maternal diet modification (without suspicion of CMPA as above), probiotic or herbal supplements and manipulation including spinal manipulation and cranial osteopathy (NICE, 2017).

ICON and preventing abusive head trauma
The current incidence of abusive head trauma remains at 20-24/100 000 (Kemp, 2011). Results of serious case reviews have shown the crying is often the final trigger for a baby being shaken (Barr et al., 2000). Previous research has shown that public health campaigns in the form of parental education in managing their infant's crying can reduce rates of abusive head trauma by up to 75% (Dias et al., 2005).
ICON is a programme of interventions aimed at supporting parents through periods of crying and subsequently preventing abusive head trauma. They have a helpful mnemonic that can be seen in Fig. 2 (ICON, 2018). The message of ICON links back to the crying curve -that infant crying is normal and will resolve (Rattray et al., 2019;Suzanne Smith, 2000, personal communication).
A series of possible opportunities for education is suggested. These include both in the antenatal and immediate postnatal period and then subsequent visits and contacts with the family (Rattray et al., 2019). For the programme to be of full benefit there should be a team approach. The message should be redelivered at each contact, therefore involving the input of midwives, health visitors, general practitioners and social workers.
For a GP, the 6-8 week baby review would be a well-timed check as this coincides with the natural peak of infant crying. Following a successful pilot by the Hampshire Clinical Commissioning Group, a template has been produced to assist practitioners in the maternal postnatal 6-8 week Reproduced with permission from Dr Suzanne Smith, ICON check. It includes screening for infant crying and educating families on the ICON message (Rattray et al., 2019). ICON is endorsed by the RCGP and is now part of the RCGP Toolkit.

Useful resources
Useful resources to refer parents or carers: . ICON -the website also has helpful videos and leaflets (ICON, 2018) . NHS Choices -clear information for parents on the management of infantile colic (NHS, 2018) . CRYSIS -website and helpline for parents or carers (CRYSIS, 2020) When to refer?
NICE have published guidance on when a presentation with a crying baby would warrant referral to secondary care. First, if there are concerns about excessive crying that is worsening or not resolving after 4-months of age. Second, if there is suspicion of an underlying cause that cannot be managed in primary care. Finally, if the parents or carers are unable to cope, despite being given reassurance and support (NICE, 2017). An urgent or same-day referral may be required if any red flag features are present. This includes if there are any safeguarding concerns where involvement from social services or local child safeguarding teams should be sought.

KEY POINTS
. The length of time a baby spends crying is often increased between the ages of 2-weeks and 4-months, with the peak of infant crying at 6-8 weeks .
In the majority of presentations of infant crying no cause is found. A thorough history and examination is important to rule out pathological causes . High infant crying can be immensely stressful for parents and carers alike, and has been found to be a risk factor for abusive head trauma . The mainstay of management of normal infant crying or colic involves reassurance, conservative soothing techniques and parental support . Antenatal and postnatal contact with caregivers can be used as an opportunity to offer support and education on infant crying.